Genomics of the relict species Baronia brevicornis sheds light on its demographic history and genome size evolution across swallowtail butterflies

Abstract

Relict species, like coelacanth, gingko, tuatara, are the remnants of formerly more ecologically and taxonomically diverse lineages. It raises the questions of why they are currently species-poor, have restrained ecology, and are often vulnerable to extinction. Estimating heterozygosity level and demographic history can guide our understanding of the evolutionary history and conservation status of relict species. However, few studies have focused on relict invertebrates compared to vertebrates. We sequenced the genome of Baronia brevicornis (Lepidoptera: Papilionidae), which is an endangered species, the sister species of all swallowtail butterflies, and is the oldest lineage of all extant butterflies. From a dried specimen, we were able to generate both long-read and short-read data and assembled a genome of 406 Mb for Baronia. We found a fairly high level of heterozygosity (0.58%) compared to other swallowtail butterflies, which contrasts with its endangered and relict status. Taking into account the high ratio of recombination over mutation, demographic analyses indicated a sharp decline of the effective population size initiated in the last million years. Moreover, the Baronia genome was used to study genome size variation in Papilionidae. Genome sizes are mostly explained by transposable elements activities, suggesting that large genomes appear to be a derived feature in swallowtail butterflies as transposable elements activity is recent and involves different transposable elements classes among species. This first Baronia genome provides a resource for assisting conservation in a flagship and relict insect species as well as for understanding swallowtail genome evolution.